The precipitous decline of the ortolan bunting Emberiza hortulana: time to build on scientific evidence to inform conservation management

The precipitous decline of the ortolan bunting

Emberiza hortulana: time to build on scientific

evidence to inform conservation management

M y l e s H . M . M e n z and R a p h a e¨ l A r l e t t a z

Abstract In recent decades there has been a marked decline

in most ortolan bunting Emberiza hortulana populations in temperate Europe, with many regional populations now extinct or on the brink of extinction. In contrast, Mediter-ranean and, as far as we know, eastern European popula-tions seem to have remained relatively stable. The causes of decline remain unclear but include: habitat loss and degra-dation, and related reduction in prey availability; climate change on the breeding grounds; altered population dynam-ics; illegal captures during migration; and environmental change in wintering areas. We review the current knowledge of the biology of the ortolan bunting and discuss the pro-posed causes of decline in relation to the different population trends in temperate and Mediterranean Europe. We suggest new avenues of research to identify the factors limiting ortolan bunting populations. The main evidence-based conservation measure that is likely to enhance habitat quality is the creation of patches of bare ground to produce sparsely vegetated foraging grounds in invertebrate-rich grassy habitats close to breeding areas.

Keywords Agricultural intensification, Emberiza hortulana, farmland birds, habitat degradation, migration, ortolan bunting, species decline, threatened species

Introduction

M

igratory birds, in particular long-distance migrants, are vulnerable to environmental change in multiple regions (Sanderson et al., 2006; Both et al., 2010). The

ortolan bunting Emberiza hortulana is the only long-distance trans-Saharan migrant among old world buntings (Cramp & Perrins, 1994; Glutz von Blotzheim & Bauer, 1997). The species has undergone the second most pro-nounced decline of any bird species in temperate Western Europe in recent decades, with an estimated 82% popula-tion reducpopula-tion between 1980 and 2008 (Klvanova et al., 2010), although the decline began earlier in some places (Conrads, 1977; Lang et al., 1990; Meier-Peithmann, 1992; Dale, 1997). Ortolan bunting populations have recently crashed across northern Europe and Scandinavia (van Noorden, 1991, 1999; Vepsa¨la¨inen et al., 2005; Ottvall et al., 2008) and the species has effectively become extinct as a breeding species within the last decade in Belgium, The Netherlands (van Noorden, 1991, 1999; Vieuxtemps & Jacob, 2002; van Dijk et al., 2005) and Switzerland (Revaz et al., 2005; Menz et al., 2009b), with mostly unpaired singing males remaining in these populations. The species has apparently remained stable in Eastern Europe (BirdLife International, 2004), and the only notable increase has been in Catalonia, in the Mediterranean (Pons, 2004; Brotons et al., 2008).

Although the life history of the ortolan bunting is generally well resolved we lack consolidated information about the species’ key ecological requirements and most con-servation action for the species is based on expert opinion rather than scientific evidence. Thus, there is uncertainty about the optimal conservation measures to implement. Given the challenges of integrating research programmes across regions and countries clear direction is required for appropriate conservation research for the ortolan bunting. In this review we: (1) synthesize existing knowledge of the biology of the ortolan bunting, (2) discuss the proposed causes of the species’ decline, (3) propose priorities for future research to inform conservation action, and (4) provide preliminary evidence-based management recommendations from the in-formation currently available (Pullin & Knight, 2001).

Literature searches were primarily on the ISI Web of Science, the Ornithological Worldwide Literature database (OWL, 2010), and reference lists from published articles. The review of threatening processes considered articles published after 1950 as this is believed to be the year in which many population declines began (Lang et al., 1990; Meier-Peithmann, 1992; Dale, 1997).

MYLES H.M. MENZ* (Corresponding author) and RAPHAE¨ L ARLETTAZy

Division of Conservation Biology, Institute of Ecology and Evolution, University of Bern, Baltzerstrasse 6, CH-3012 Bern, Switzerland. E-mail myles.menz@bgpa.wa.gov.au

*Also at: Kings Park and Botanic Garden, The Botanic Gardens and Parks Authority, West Perth, Western Australia, Australia, The School of Plant Biology, The University of Western Australia, Crawley, Western Australia, Australia, and Division of Evolution, Ecology and Genetics, Research School of Biology, The Australian National University, Canberra, Australian Capital Territory, Australia

y

Also at: Swiss Ornithological Institute, Valais Field Station, Nature Centre, Salgesch, Switzerland

Received 21 August 2010. Revision requested 4 November 2010. Accepted 4 January 2011. First published online 2 December 2011.

Ecology of the ortolan bunting Habitat requirements

In Mediterranean and sub-Mediterranean Europe the species breeds primarily in open shrubland and steppe-like habitat, particularly on south-facing slopes (Cramp & Perrins, 1994; Glutz von Blotzheim & Bauer, 1997; Fonderflick et al., 2005; Brotons et al., 2008). Here, the species favours areas with shrub and tree cover of c. 20–30% (Ko¨lsch, 1959; Keusch, 1991; Menz et al., 2009a) and rarely occurs where tree cover exceeds 30–50% (Fonderflick et al., 2005; Fonderflick, 2006). In temperate Europe the species breeds primarily in agricultural habitats, particularly areas of small-scale cultivation, set-asides, short-rotation coppice and shrublands in historically burnt habitats, with these habitats often co-occurring (e.g. Berg & Pa¨rt, 1994; Dale & Hagen, 1997; Berg, 2002; Dale & Olsen, 2002; Go1awski & Dombrowski, 2002; Revaz et al., 2005). In farmland the species favours field margins with structural elements such as isolated trees, hedges and nearby forest margins (Meier-Peithmann, 1992; Gru¨tzmann et al., 2002), a characteristic shared by several farmland bunting species (Brambilla et al., 2008, 2009).

Within both natural and agricultural landscapes the ortolan bunting breeds primarily in relatively warm, dry areas, with well-drained soils and an annual rainfall below 600–700 mm (Cramp & Perrins, 1994; Gru¨tzmann et al., 2002), avoiding wet habitats (e.g. Nævra, 2002; Dale & Manceau, 2003; Ha¨nel, 2004; Deutsch, 2007). Exceptions include populations occurring in areas with extremely well-drained soils and steep, sloping topography (Conrads, 1977). Ortolan buntings nest on the ground, typically producing only one brood per season, with exceptional replacement clutches and second broods (Garling, 1943; Conrads, 1969; Ha¨nel, 2004).

Ortolan bunting populations typically consist of loose aggregations of breeding pairs (Vepsa¨la¨inen et al., 2007). Local colonization, extinction, and population fluctuations are often observed (Glitz, 1967; Dale & Steifetten, 2011), with areas seemingly isolated from other populations also colonized (van Noorden, 1991, 1999; Revaz et al., 2005). This could indicate the existence of a broadscale metapopulation structure, with areas being settled or abandoned as habitat suitability fluctuates following major disturbance events (Brotons et al., 2005). Short-term population increases have been observed in response to fire (Brotons et al., 2005, 2008), clearing of vegetation by a storm, forestry inter-ventions, or cultivation (Conrads & Kipp, 1980; Nævra, 2002). Sparse vegetation and a large proportion of bare ground are the most noticeable common features of these habitats (Nævra, 2002). The species often becomes locally common after disturbance (Sposimo, 1988; Pons, 2004; Revaz et al., 2005) with, for example, populations peaking

3–4 years after fire (Pons & Clavero, 2010). This relation-ship is particularly strong in Mediterranean and, to a lesser extent, sub-Mediterranean biomes, where occurrence of fires is still commonplace, and it is also noticeable in temperate Europe where the species also nests on historic burns (e.g. Dale & Olsen, 2002; Revaz et al., 2005). This indicates that the ortolan bunting behaves like a pioneer species, typically colonizing the early stages of vegetation succession.

Diet

The ortolan bunting has a varied diet, including both plant (seeds) and animal matter (Cramp & Perrins, 1994; Glutz von Blotzheim & Bauer, 1997), although the diet of the chicks is restricted to a few dominant prey orders: Lepi-doptera, particularly Tortricidae larvae, and Coleoptera in the north of its range (Conrads, 1968, 1969; Ha¨nel, 2004), and Orthoptera, particularly Tettigoniidae, in the south (Kunz, 1950; Keusch & Mosimann, 1984). In Switzerland, Tettigoniidae made up nearly 70% of the total items provisioned to nestlings, a much higher percentage than in the sympatric rock bunting Emberiza cia, which has a more diverse diet (Keusch & Mosimann, 1984). In the north of the range caterpillars are fed to nestlings in the early stages of development, with diet switching towards larger prey in later developmental stages until post-fledging (Kunze, 1954; Knoblauch, 1968; Conrads, 1969; Ha¨nel, 2004).

Foraging ecology

Ortolan buntings forage primarily in patches of

bare ground within sparsely vegetated habitats (Stolt, 1974; Gnielka, 1987; Boitier, 2001; Menz et al., 2009b). However, prey such as caterpillars are also collected from fields (Conrads, 1969), or gleaned from tree crown foliage, particularly oaks Quercus spp. (Knoblauch, 1968; Conrads, 1969; Stolt, 1974; Gnielka, 1987), which harbour a relatively high density of caterpillars compared to other tree species (Naef-Daenzer, 2000). Adult males sometimes forage in the same oaks used as song posts (Ha¨nel, 2004). Consequently, song post selection may function as a signal of territory quality, as oaks appear to be over-represented as song posts, compared to local availability of other tree species (M.H.M. Menz, pers. obs.).

In Switzerland most Tettigoniidae fed to nestlings are captured on the ground (Keusch & Mosimann, 1984) and in Germany Coleoptera are collected on paths or in cereal fields (Knoblauch, 1968). Tettigoniidae are most abundant in relatively dense steppe grass or bushes (Arlettaz et al., 1997). However, ortolan buntings do not necessarily forage in habitats with highest prey abundance but rather in those with a high proportion of bare ground (Menz et al., 2009b), as observed in other ground foraging birds (Wilson et al.,

2005; Schaub et al., 2010). Prey accessibility, therefore, rather than abundance, drives foraging habitat selection (Menz et al., 2009b; Schaub et al., 2010).

In temperate Europe foraging often takes place in cultivated fields, sometimes a distance away from breeding areas (Dale, 2000; Dale & Olsen, 2002). Cereal fields, particularly oats, are important for replenishing body fat prior to and upon return from migration, when birds feed on seeds and sprouting plants (Keusch, 1991; Gru¨tzmann et al., 2002). Oat is probably favoured because of the high energy content of the grain (Glutz von Blotzheim, 1989; Diaz, 1990). Threats and reasons for decline

Habitat loss and degradation, and reduction in prey availability

Agricultural intensification has resulted in land-use changes such as homogenization of agricultural landscapes, loss of structural heterogeneity and an increased use of pesticides (Newton, 2004). A reduction of crop diversity and the transition in cultivation from summer to winter cereals may have contributed to the decline of the ortolan bunting, as such changes will limit the amount of bare ground in cultivated fields. Conversion of rye, and espe-cially oat, to maize cultures has been reported to affect the species negatively (Maes et al., 1985; Ikemeyer & von Bu¨low, 1995; van Noorden, 1999; Gru¨tzmann et al., 2002; Deutsch, 2007; Berg, 2008), although this has not been quantified. Creation of monoculture agricultural habitats by destruc-tion of structural habitat elements such as tree lines and hedges may be detrimental, as these provide song posts and foraging opportunities (Knoblauch, 1968; Vepsa¨la¨inen et al., 2005). Urbanization has often encroached into small-scale agricultural areas that had typically been preserved close to villages (van Noorden, 1999), increasing disturbance near to breeding areas (Steiner & Hu¨ni-Luft, 1971).

One of the principal reasons for the observed decline of the ortolan bunting in temperate Europe is probably a re-duction in prey availability/accessibility driven by habitat deterioration on the breeding grounds, primarily via changes in agricultural practices (Claessens, 1992; Kutzenberger, 1994; van Noorden, 1999; Gru¨tzmann et al., 2002; Revaz et al., 2005; Vepsa¨la¨inen et al., 2005; Deutsch, 2007). A reduction in patches of bare ground within foraging areas will result in decreased prey availability (Wilson et al., 2005; Schaub et al., 2010) in two ways. Firstly, agricultural in-tensification includes increased application of fertilizers, which closes the vegetation and suppresses patches of bare ground, and the use of pesticides eliminates invertebrate prey. Secondly, areas of bare ground also vanish following vegetation encroachment through natural succession after abandonment of traditional agricultural practices such as extensive grazing and burning of dry grass (Stolt, 1974; Dale,

1997; Nævra, 2002; Revaz et al., 2005; Wilson et al., 2005; Sirami et al., 2007; Menz et al., 2009b; de Groot et al., 2010). There is increasing evidence that reduction in structural heterogeneity and bare ground is threatening a number of ground-foraging farmland bird species (Wilson et al., 2005; Schaub et al., 2010).

Climate change on the breeding grounds

Climate change has been proposed as a possible cause of the decline of the ortolan bunting (Knoblauch, 1954; Helb, 1974; Maes et al., 1985; Gru¨tzmann et al., 2002; Vieuxtemps & Jacob, 2002). A low tolerance to cold temperatures (Wallgren, 1952, 1954) may increase the risk of physiological stress on breeding birds during inclement weather. Micro-climate at the nest site is also likely to have consequences for the growth and survival of the nestlings (Conrads, 1977; Lang et al., 1990; Dale, 2000; Dale & Olsen, 2002; Gru¨tzmann et al., 2002; Vepsa¨la¨inen et al., 2005), as observed in other bird species (Ullrich, 1971). Poor weather during the breeding season, such as cold, rainy springs, also lowers reproductive success through nestling mortality from food limitation (Ruge et al., 1970; Fonderflick & The´venot, 2002), something also observed in other species (Arlettaz et al., 2010).

The earlier growing season predicted under some climate change scenarios may lead to reduced foraging opportunities for ortolan buntings returning to their breed-ing grounds because of vegetation closure (Lang, 2007). The relatively short nestling phase (9–14 days; Cramp & Perrins, 1994; Glutz von Blotzheim & Bauer, 1997) means chicks require a large amount of invertebrate prey in a short period (Meier-Peithmann, 1992). Ortolan buntings may have evolved a reproductive phenology to coincide with peak prey availability, as seen in some other bird and mammal species (Blondel et al., 1991; Arlettaz & Fournier, 1993; van Noordwijk et al., 1995; Arlettaz et al., 1997, 2001). Chicks usually hatch in c. mid June, when Tettigoniidae are abundant and at a profitable size (Kunz, 1950; Arlettaz et al., 2001). Conrads (1968, 1977) noted breeding was synchronous with sprouting of oak leaves and the appearance of large numbers of defoliating caterpillars, although this was not quantified. Given the short breeding season and nestling phase, and their relatively late return from Africa (Claverie, 1955), altered climate regimes may see a mismatch between breeding period and prey availability (Both et al., 2010). Altered population structure and dynamics

Studies from multiple regions have reported 29–60% of singing ortolan bunting males remain unpaired during the breeding season (Conrads, 1968; Dale, 2001; Fonderflick & The´venot, 2002; Steifetten & Dale, 2006; Berg, 2008). However, even in declining and fluctuating populations

breeding success appears to remain stable (Maes, 1989; Steifetten & Dale, 2006). In small and isolated populations unpaired males may be all that remain prior to population extinction (Dale, 2001; Vieuxtemps & Jacob, 2002; Donald, 2007; Menz et al., 2009b). In Norway populations are limited by a drastic reduction in the number of breeding pairs because of females dispersing away from the population (Dale, 2001; Steifetten & Dale, 2006), resulting in the male-biased sex-ratio seen in declining populations (Dale et al., 2006). In relatively isolated populations there is little opportunity for recruitment of females from elsewhere (Steifetten & Dale, 2006). Declines and local population fluctuations are also driven by males undertaking relatively long-distance breeding dispersal in search of females (Dale et al., 2005; Dale & Christiansen, 2010; Dale & Steifetten, 2011). Loss of females from a population can only be mitigated by increasing the availability and suitability of habitat patches within breeding areas, which requires de-tailed knowledge of the species’ habitat and foraging require-ments (Steifetten & Dale, 2006).

Illegal captures during migration

The ability to constitute fat reserves rapidly before autumn migration seems to be an idiosyncrasy of the ortolan bunting, a characteristic known for centuries in gastro-nomic circles around Europe (Bastien, 1798; Kumerloeve, 1954; Claverie, 1955). The fact that the ortolan bunting is the only species of bunting in Western Europe that undertakes long-distance migration may indicate specific adaptations for storing fat reserves. Historically, large numbers of ortolan buntings were trapped during the autumn and, to a lesser extent, spring migration, mostly in southern Europe (Claessens, 1992). Small traps known as matoles are used that are baited exclusively with nearly ripe oat stalks (Claverie, 1955). It is likely that the species has become a delicacy because of its propensity to lay down fat relatively quickly when fed grain (oat and millet) ad libitum in captivity (Claverie, 1955; Claessens, 1992; Dale, 1997; Steifetten & Dale, 2006). After fire a wild form of oat occurs en masse in some Mediterranean habitats (R. Arlettaz, unpubl. data) and may have constituted an important food source prior to the expansion of agriculture.

In some areas of south-west France, despite the species now being protected, trapping and fattening continues unabated, with an estimated 50,000 birds illegally captured per year until at least the early 1990s (Claessens, 1992). No studies have been conducted on the consequences of this regionally intensive poaching on the demography of temperate European popula-tions. Although it is unlikely that birds from all declining European populations of the ortolan bunting cross these areas during migration, in a wide-scale metapopulation system these losses may affect overall population dynamics and thus also have regional consequences for distant populations.

Environmental changes in wintering areas

Although the migration phenology is well documented for Europe (Stolt, 1977; Cramp & Perrins, 1994; Stolt & Fransson, 1995; Yosef & Tryjanowski, 2002; Bairlein et al., 2009), the wintering areas of the ortolan bunting are poorly known. Habitat changes in wintering areas because of climate variation and/or anthropogenic impacts on land (e.g. pesticides, Vepsa¨la¨inen et al., 2005; Zwarts et al., 2009)

may also contribute to the observed population

declines (Conrads, 1977; Kutzenberger, 1994; Busche, 2005; Vepsa¨la¨inen et al., 2005; Lang, 2007). However, the fact that some populations in the Mediterranean have been recently expanding (Brotons et al., 2008) seems to indicate that the problem may lie primarily with the quality of the breeding grounds in Europe, possibly compounded by environmental changes in African wintering areas. Identi-fication of the wintering areas of this species is imperative for understanding factors that may be affecting the species outside the breeding season and whether birds from temperate and Mediterranean populations winter in different areas.

Discussion

Knowledge gaps and recommendations for future research

Further information on the diet of the ortolan bunting across its range, particularly quantification of nestling diet in relation to prey availability in the main foraging habitats, is required for a full understanding of the species’ ecological requirements. In particular, quantification of the abun-dance and availability (the latter being abunabun-dance modified by accessibility) of major invertebrate groups in relation to the stages of vegetation succession following events such as fire may provide information on why the species colonizes these disturbed habitats during specific time windows (Pons & Clavero, 2010). Understanding the relationships between timing of breeding and prey phenology/availability would also elucidate the potential effects of weather and climate variation on reproductive output. Shifts in insect phenology could potentially lead to a mismatch between breeding season and prey availability, a phenomenon that may particularly affect long-distance migrants (Both et al., 2010).

More data are required on survival and movement patterns in areas where populations are stable (Pons, 2004). As most detailed studies on population structure and dynamics have been conducted in northern Europe (particularly Norway: Dale, 2001; Steifetten & Dale, 2006; Dale & Steifetten, 2011), a comparison between eastern European, Mediterranean and temperate populations would facilitate an understanding of the demographic

factors limiting populations, such as the propensity for females to disperse away from certain areas. Investigation into the extent of continued poaching would elucidate the potential effects this may have on the demography of temperate European populations as a whole.

Climate variation has already affected the ecology and distribution of some bird species (Arlettaz et al., 2010; Both et al., 2010). It is uncertain what effect predicted climate change scenarios would have on the ortolan bunting, especially given the paucity of data on future precipitation regimes (Easterling et al., 2000) and the impact of weather on the species’ reproductive success. Studies at the edges of the species’ range could provide insights into possible colonization of higher latitudes and altitudes. In Mediter-ranean Europe temperature increases may lead to aban-donment of the warmest areas. Such studies are needed to disentangle the future effects of climate modification and ecosystem changes. Identification of the species’ African wintering grounds by use of new light-weight tracking techniques such as geolocators (Ba¨chler et al., 2010) would facilitate the assessment of any potential environmental issues that may be contributing to the decline of the species outside its breeding areas and elucidate the connectivity of European breeding populations.

Conservation recommendations

Until we know more about the specific factors limiting ortolan bunting populations, we recommend application of evidence-based conservation measures (Pullin & Knight, 2001) to counteract vegetation encroachment and increase the proportion of patches of bare ground within vegetated patches close to ortolan bunting breeding areas. This could be achieved through extensive grazing, controlled fire (Wilson et al., 2005; Schaub et al., 2010) and forestry interventions such as short-rotation coppicing (Berg, 2002). However, attention should be paid to protecting sufficient dense grass sward to support prey populations. Patches of bare ground in cultivated fields close to breeding areas may also be produced by spring sowing, decreasing seed sowing density or increasing the distance between rows in sown fields. Although prescribed fire may be a cost-effective management option that is already used in several countries to counteract vegetation encroachment (Montane´ et al., 2009), further research is required to determine the potential detrimental effects of prescribed burning on other aspects of biodiversity. In southern Switzerland extensive grazing, forestry measures (coppicing), sowing of oat fields and controlled fire have recently been applied simulta-neously to halt the decline of a rare butterfly species and the ortolan bunting (E. Revaz & R. Arlettaz, unpubl. data). Thus in certain habitats conservation measures targeting the ortolan bunting may have broader benefits for biodiversity.

Acknowledgements

We acknowledge O. Roth and C. Marti for assisting with sourcing literature. V. Braunisch, T. Reichlin and M. Berman assisted with translation of German and French literature. MHMM was supported by an Australian Post-graduate Award, and grants from the Holsworth Wildlife Research Endowment and the School of Plant Biology at the University of Western Australia. We also thank R.D. Phillips and two anonymous referees for their constructive comments.

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Biographical sketches

MY L E S ME N Z has a broad interest in landscape ecology and conservation biology of birds, insects and plants, with particular interest in pollination ecology and the restoration of plant-pollinator mutualisms. RA P H A E¨ L AR L E T T A Z has wide interests in biodiversity conservation. His research is aimed at providing the necessary rigorous evidence-based guidance to maintain and re-store ecosystems and their emblematic species, especially verte-brates and inverteverte-brates in agro-ecosystems and Alpine ecosystems. He is also committed to bridging the great divide that exists between research and action in conservation biology, developing integrated research-implementation programmes, mostly within Switzerland.